Exertional dyspnea in athletes

Full text

BC MEDICAL JOURNAL VOL. 45 NO. 10, DECEMBER 2003
508
ABSTRACT: Exertional dyspnea in
active patients can be challenging
to diagnose and to treat. While
exercise-induced asthma (EIA) is
the most common cause of exer-
tional dyspnea in athletes, two less
common causes—vocal cord dys-
function and pulmonary embolism—
should also be considered. These
less common causes of exertional
dyspnea require treatments unlike
those used for EIA. In addition, they
may represent more significant
health risks, and should be included
in any differential diagnosis of exer-
tional dyspnea.
The most common cause of
exertional dyspnea in active
patients is exercise-induced
asthma (EIA), defined as
“an intermittent narrowing of the air-
ways, accompanied by a decrease in
some measure of airflow that the indi-
vidual experiences as wheezing, chest
tightness, coughing, and dyspnea that
is triggered by exercise.”1Up to 90%
of chronic asthma patients can experi-
ence exercise-induced asthma during
the course of their disease.2Exercise-
induced asthma seems to have an
increased prevalence in more athletic
populations.3The symptoms of EIA
include the typical asthma symptoms
mentioned above, and may also in-
clude poor performance for a given
level of conditioning, or performance
changes that are season- and climate-
related.
Transient airway narrowing dur-
ing and following exercise causes
exercise-induced asthma symptoms.
These symptoms may last 1 to 2 hours
following the cessation of exercise.
High ventilatory rates during exercise
lead to evaporative water loss of air-
way surface liquid. This process leads
to cooling and changes in osmolarity
of the airway surface liquid that trig-
gers the inflammatory mediators that
cause smooth muscle constriction and
airway edema.
Diagnosis of EIA
Diagnosis of EIA can often be chal-
lenging. History-taking focuses on
respiratory symptoms, family history,
and environmental and activity trig-
gers. In sport there are some unique
precipitating factors worth consider-
ing. These include the cold, dry envi-
ronment of Nordic skiing, chlorine in
swimming pools, and pollution from
ice resurfacing machines. The physi-
cal examination is often normal at rest.
If the patient has incompletely treated
baseline asthma, the exam may in-
clude wheezing, end-inspiratory cough-
ing, and a prolonged expiratory phase.
Resting spirometry may also be normal.
Historically, the best test of exer-
cise-induced asthma has been a com-
bination of spirometry and a field
challenge.3The field challenge should
be similar in intensity and environ-
Exertional dyspnea
in athletes
The shortness of breath experienced by some active individuals
does not always have a straightforward pathophysiology.
M. Koehle, MD, D.R. Lloyd-Smith, MD, D.C. McKenzie, MD, PhD
Dr Koehle is a physician at the Allan
McGavin Sports Medicine Centre and St.
Paul’s Hospital, and a clinical instructor fel-
low in the Department of Family Practice at
the University of British Columbia. Dr
Lloyd-Smith is a primary care physician at
the Allan McGavin Sports Medicine Centre
and a clinical professor in the School of
Human Kinetics, UBC. Dr McKenzie is a
physician at the Allan McGavin Sports Med-
icine Centre and a professor of Human Ki-
netics at the University of British Columbia.

VOL. 45 NO. 10, DECEMBER 2003 BC MEDICAL JOURNAL 509
ment to the athlete’s typical exercise
situation. For example, if a cross-
country skier with possible EIA per-
forms treadmill exercise in a warm,
humid lab, there may be no changes
on spirometry, thus leading to a false-
negative result. The combination of
field challenge and spirometry can be
logistically difficult to undertake, and
therefore a number of surrogate tests
have been developed in an attempt to
diagnose EIA more conveniently.
Provocative tests for EIA include
pharmacologic challenge tests, volun-
tary hyperventilation, and osmotic
challenge tests. Chemical challenge
tests such as methacholine and his-
tamine challenge are useful in the
diagnosis of chronic asthma. When
compared with spirometry and field
challenge, pharmacologic challenge
tests appear to be more sensitive for
airway reactivity, but much less spe-
cific for exercise-induced asthma.3
Voluntary hyperventilation tests at-
tempt to mimic the high minute venti-
lation that occurs during exercise. The
eucapnic voluntary hyperpnoea (EVH)
test uses mixed gases to maintain iso-
capnia while the patient ventilates at a
level consistent with exercise. Spiro-
metry is performed after the hyper-
ventilation to assess for airflow limi-
tation. When compared with field
challenge and spirometry, EVH test-
ing demonstrates improved sensi-
tivity and specificity.4Research has
recently been done with respect to
osmotic challenge tests. Either hyper-
tonic saline or mannitol in an inhaled
form is used to provoke an asthmatic
response. At present, these tests show
some promise as alternative diagnos-
tic tests for EIA, but more research
needs to be done. In summary, al-
though a combination of field chal-
lenge and spirometry is regarded as
the gold standard for EIA, it can
be inconvenient or logistically diffi-
cult. EVH testing is an alternative that
is preferred by the International Oly-
mpic Committee.
Treatment of EIA
Treatment can be divided into phar-
macologic and nonpharmacologic
strategies. The simplest nonpharma-
cologic treatment is to choose activi-
ties and environments that are less
asthmogenic. Ideally, a warm humid
environment is best. Activities that do
not involve high ventilatory rates are
best for patients with EIA. These
include baseball, football, golf, gym-
nastics, martial arts, sprinting, swim-
ming, tennis, weightlifting, and water
polo.5,6 Another effective tactic for
attenuating EIA attacks is the imple-
mentation of an effective warm-up.
An appropriate warm-up is 15 min-
utes of activity prior to the practice or
competition. The exercise intensity
should be such that it does not induce
bronchospasm.
When considering pharmacologic
treatment of exercise-induced asthma,
it is important to ensure that underly-
ing asthma is treated sufficiently to
ensure normal baseline spirometry.
Once normal baseline spirometry is
established, medications can be ad-
ministered before exercise to prevent
an exercise-induced attack. If treating
competitive athletes, the prescribing
physician should be aware of the dop-
ing regulations for the athlete’s partic-
ular sport. Some asthma medications
are banned, while others require labo-
ratory documentation of the patient’s
condition.7lists restricted
medications.
The most common pharmacologic
strategy is to take a short-acting beta-
agonist (such as salbutamol) 30 to
60 minutes before exercise. These
Table 1
Exertional dyspnea in athletes
Table 1. Summary of restricted medications in the treatment of asthma.
Banned substances Permitted in certain circumstances
Bambuterol (†Bambec, †Oxeol) *Formoterol (efformoterol, Foradil,
Oxeze-Turbuhaler, †Oxis)
Clenbuterol (†Broncoterol, †Spiropent, *Salbutamol (Albuterol, Alti-, Nu-, Med-,
Ventipulmin [veterinary]) Dom-Salbutamol, Apo-Salvent, Ventolin,
Novo-Salmol, Airomir, Salbu-2, -4, Asmavent,
Combivent, Ventidisk, Sabulin)
Fenoterol (Berotec, Duovent UDV) *Salmeterol (Serevent)
Isoproterenol (isoprenaline, Isuprel) *Terbutaline (Bricanyl Turbuhaler, †Brethine)
Orciprenaline (metaproterenol, Apo-, Alti-, *Glucocorticosteroids administered as an
Tanta-Orciprenaline) inhaler
Reproterol (†Bronchospamin)
*Permitted only by inhalation. Athletes must provide written declaration to the relevant medical author-
ity in advance of a doping control test or competition. Written declaration should be made at the time
the medication is prescribed. (N.B. Athletes who give notification of the intent to use an inhaled, per-
mitted beta-2 agonist at the 2004 Summer Olympic Games will now be required to submit clinical and
laboratory evidence that justifies the treatment and will be assessed by an independent medical
panel.)
†Other brand names used outside Canada.
Montelukast, zafirlukast, cromolyn sodium, sodium cromoglycate, nedocromil and ipratropium are
all permitted if needed to treat a justifiable medical condition.
Source: Compiled from data on the Canadian Centre for Ethics in Sport web site at www.cces.ca.

BC MEDICAL JOURNAL VOL. 45 NO. 10, DECEMBER 2003
510
medications can also be taken as “res-
cue” medications after exercise to re-
duce symptoms in the event of an at-
tack. There has been some concern
about the long-term frequent use of
short-acting beta-agonists leading to
diminished effectiveness.6For this
reason, other medications can be pre-
scribed to decrease the frequency of
beta-agonist usage. These include
inhaled corticosteroids, long-acting
beta-agonists, mast cell stabilizers,
and leukotriene antagonists. None of
these alternate medications can be
used as a rescue medication to abort
an attack. Both inhaled corticosteroids
and long-acting beta-agonists are effec-
tive in attenuating exercise-induced
asthma.6Inhaled corticosteroids such
as fluticasone and budesonide need to
be taken for several weeks to be effec-
tive. Leukotriene antagonists (mon-
telukast and zafirlukast) are partially
effective in attenuating EIA, and last
for at least 8 hours, making them an
effective adjunct treatment, especially
in patients who are exercising more
than once a day. Mast cell stabilizers
such as necrodomil sodium and cro-
molyn sodium are less effective than
beta-agonists in preventing EIA, but
may have a role in patients who are
unable to take beta-agonists. In sum-
mary, short-acting beta-agonists taken
30 to 60 minutes before activity are
the mainstay of pharmacologic treat-
ment of EIA. Other agents such as in-
haled corticosteroids, long-acting beta-
agonists, and leukotriene antagonists
can be used as adjunct treatments to
decrease the need for short-acting
beta-agonists.
Exercise-induced asthma is a com-
mon condition affecting many asthma-
tics. Clinical findings in the office are
often few, and there is no reliable, con-
venient laboratory test to confirm the
diagnosis. Fortunately, there are a num-
ber of pharmacologic and nonpharma-
cologic strategies that can be imple-
mented to reduce the frequency and
severity of EIA episodes. In fact, many
Olympic medals in highly aerobic
sports such as swimming have been
won by athletes with severe asthma
that has been controlled with the above
strategies.7Consequently, properly treat-
ed EIA does not hinder performance.
Conditions that mimic EIA
The following cases serve to illustrate
two less common conditions that
occur in high-performance athletes.
Both pulmonary embolism and vocal
cord dysfunction can mimic EIA, thus
it is always useful to consider them in
the diagnosis of active patients with
exertional dyspnea ( ). Unlike
exercise-induced asthma, these enti-
ties can limit performance, and may
represent significant health risks.
Case 1
A 25-year-old elite cross-country
skier presented with a 2-week history
of increasing shortness of breath on
exertion. Her symptoms resembled a
previous episode approximately 2
years before that had resolved after a
hiatus in training. Three years before,
the patient had been given a diagnosis
of exercise-induced asthma (EIA), for
which she was prescribed salmeterol
and fluticasone for exacerbations.
Approximately 1 week before presen-
tation, she had restarted her fluticas-
one and salmeterol, and had intro-
duced loratidine. The patient also had
a history of pneumonia approximate-
ly 4 years earlier that had been resolved
with outpatient antibiotic therapy.
Previously, this athlete had been
tested for allergies and had reacted to
dogs, feathers, dust mites, trees, and
moulds. There was no history of ASA
sensitivity. She was a nonsmoker and
otherwise healthy. Her only medica-
tion was a triphasic estrogen/progestin
oral contraceptive.
On examination she was in no vis-
ible distress. There was no evidence
of clubbing or cyanosis. Pulse was 76
and regular; blood pressure was 120/80.
Auscultation of lung fields revealed
good air entry and no abnormal breath
sounds. Cardiovascular examination
revealed normal S1and S2with no
murmurs or extra heart sounds. The
rest of the physical examination was
normal. Spirometry and methacholine
challenge were performed. Both were
within normal limits.
Table 2
Exertional dyspnea in athletes
Table 2. Clinical findings of exercise-induced asthma, vocal cord dysfunction,
and pulmonary embolism.
Clinical finding Exercise-induced Vocal cord Pulmonary
asthma dysfunction embolism
Exertional dyspnea + + +
Chest pain +/– – +/–
Inspiratory stridor – + –
Expiratory limitation + – –
Arterial desaturation +/– +/– ++
Response to b-agonists + – –
Abnormal spirometry +/– +(during exercise)/– –

VOL. 45 NO. 10, DECEMBER 2003 BC MEDICAL JOURNAL 511
The patient was referred for an
exercise study to assess for exercise-
induced asthma. The study failed to
show any evidence of obstruction.
While exercising, her hemoglobin sat-
uration dropped from 99% to 79%. An
urgent ventilation/perfusion scan was
obtained. The scan demonstrated mul-
tiple segmental defects bilaterally af-
fecting approximately 40% of her pul-
monary vasculature ( ). She was
immediately admitted to hospital and
treated with anticoagulants.
Workup for hypercoagulability,
including lab tests for protein S, pro-
tein C, and factor V Leiden, demon-
strated no abnormalities. The only
identified hypercoagulable risk factor
was the use of a triphasic oral contra-
ceptive. This medication was subse-
quently stopped.
After a 3-month period of treat-
ment with oral anticoagulants, the pa-
tient returned to activity. She experi-
enced profound dyspnea and fatigue
that limited her exercise capacity at
first. This improved over the course of
6 months with a return to training and
eventually to high-level competition.
For contraception, a progestin-only
preparation was recommended.
Figure
Case 2
A 25-year-old elite track-and-field
athlete presented with a 3-year histo-
ry of exertional dyspnea. While run-
ning, she developed tightness in her
throat, with some slight chest tight-
ness. She also noticed a stridorous
sensation when breathing heavily that
resolved on cessation of running. The
symptoms seemed to be worst during
the autumn, at the same time as she
would suffer from some nasal conges-
tion and postnasal drip.
Several asthma medications were
tried, including salbutamol, salme-
terol, montelukast, and fluticasone.
These provided minimal benefit.
Formoterol appeared to offer some
improvement, but was subsequently
banned by the athlete’s regulatory
body and was discontinued. Asecond
trial of formoterol at a later date
seemed to have little beneficial effect.
The athlete had no previous com-
plaints of allergies until the year
before when she developed some peren-
nial rhinitis. There was no concom-
itant history of either urticaria or
atopic dermatitis. Allergy testing re-
vealed skin reactions to alder, maple,
and grass. Other than a history of gas-
troesophageal reflux disease and some
visual impairment, the patient had no
other medical issues. She was on no
medications other than multivitamins,
calcium, and vitamins C and E. Alife-
long nonsmoker, she did have a sig-
nificant exposure to passive smoke.
On examination, the patient was
in no apparent distress. Her pulse was
regular at 54 beats per minute. Blood
pressure was 126/92. Respiratory rate
was 14. There was no evidence of
clubbing, cyanosis, or lymphadenopa-
thy. Nasal mucosa was erythematous
and congested. Cardiovascular exam-
ination revealed normal S1and S2,
with no extra heart sounds. There was
no peripheral edema or jugular venous
distension. Auscultation of the lungs
revealed good air entry bilaterally
with no adventitial sounds. Abdomi-
nal, neurological, and endocrine ex-
aminations were unremarkable.
Spirometry was within normal lim-
its. Amethacholine challenge test was
not suggestive of underlying bron-
chial hyperreactivity. A progressive
exercise test was performed, during
which the patient developed audible
inspiratory stridor that led to a flat-
tening of the inspiratory limb on her
Exertional dyspnea in athletes
Figure. Ventilation (left) and perfusion (right) of patient in case 1, demonstrating multiple segmental perfusion defects bilaterally.

BC MEDICAL JOURNAL VOL. 45 NO. 10, DECEMBER 2003
512
flow-volume loop. Exercise was ter-
minated at this point.
The patient was diagnosed with
vocal cord dysfunction and started on
a nasal corticosteroid to reduce her
rhinitis and postnasal drip. This treat-
ment proved to be of little benefit. It
was thought that perhaps gastroe-
sophageal reflux was irritating her
upper airway and aggravating her
symptoms. A 24-hour pH study and
esophageal physiology testing were
performed. These tests demonstrated
both acid reflux and a hypotensive
lower esophageal sphincter. The pa-
tient is presently undertaking a trial of
pantoprazole to reduce her gastric acid
secretion and to reduce her upper air-
way irritation.
Discussion
Exertional dyspnea, which is common
in the young athlete, may not always
have a straightforward pathophysiol-
ogy. The two cases described here
illustrate exertional dyspnea not caused
by exercise-induced asthma. Both
pulmonary embolism and vocal cord
dysfunction are uncommon entities,
but are important in the differential
diagnosis of exertional dyspnea. These
entities can be difficult to distinguish
in the active patient. They can each
present with dyspnea on exertion,
chest tightness, and a decline in per-
formance.
Pulmonary embolism
Several cases of pulmonary embolism
in young athletes have been reported
in the literature.8-13 Although an un-
common condition in this generally
healthy population, pulmonary em-
bolism can have significant conse-
quences, and is an important diagno-
sis to consider in athletes. In the
reported cases in the literature, the
patient with pulmonary embolism had
usually been treated for a number of
other conditions before the correct
diagnosis was reached. These condi-
tions included acute bronchitis, pneu-
monia, and asthma. Early identifica-
tion of pulmonary embolism would
reduce unnecessary investigations,
treatments, and morbidity for these
patients.
Athletes have some unique possi-
ble risk factors for thromboembolism.
Some authors have suggested that the
illicit use of substances such as ana-
bolic steroids and diuretics may put
athletes at higher risk.9,13,14 In addition,
some competitive athletes such as
wrestlers and rowers opt to (ill-advis-
edly) dehydrate themselves routinely
to “make weight.” This behavior may
lead to an increase in blood viscosity,
and hence venous stasis. Similarly,
athletes who take erythropoietin to
increase the oxygen capacity of their
blood may also be increasing their
thromboembolic risk.15
Although the usual source of
thrombosis in pulmonary embolism is
the pelvic and proximal thigh veins,
athletes may be more at risk for devel-
opment of thrombus in their upper
extremities. Paget-von Schrötter syn-
drome, or effort-induced thrombosis,
denotes the formation of such a throm-
bus in the upper extremity (usually in
the axillary vein) as a result of heavy
arm use. This condition typically
occurs in throwers.16 The symptoms of
effort-induced thrombosis are those
of vascular obstruction in the upper
extremity, and include swelling, aching
pain, paresthesia, and numbness in the
distal arm. If chest symptoms occur,
then pulmonary embolism should be
considered. The pathophysiology of
effort-induced thrombosis is not well
understood, but is believed to be relat-
ed to trauma to the vessel wall, pre-
cipitating thrombosis.
The woman in the case described
above was investigated for hyperco-
agulable conditions, but all of her
results were normal. Her only identi-
fiable risk factor for thromboem-
bolism was her use of a combined oral
contraceptive preparation. The rela-
tive risk in oral contraception users of
second- and third-generation oral con-
traceptives compared with non-users
is between 3 and 6, although the ab-
solute risk is very low. In a healthy
population, the risk of thromboem-
bolism increases with oral contracep-
tive use from less than 1 per 10000
woman-years to 3 to 4 per 10000
Exertional dyspnea in athletes
Although the usual source of thrombosis
in pulmonary embolism is the pelvic and
proximal thigh veins, athletes may be more
at risk for development of thrombus in
their upper extremities.

VOL. 45 NO. 10, DECEMBER 2003 BC MEDICAL JOURNAL 513
woman-years.17,18 The relative risk of
thromboembolism for combined oral
contraceptive users is approximately
one-half of that in pregnancy.18 The
risk of thromboembolic disease is pos-
sibly higher for patients using oral
contraceptives with a third-generation
progestin (such as desogestrel, gesto-
dene, and norgestimate) than for pa-
tients using a second-generation prog-
estin (norgestrel, levonorgestrel, and
norgestrienone).18 A progestin-only
preparation such as injectable medro-
xyprogesterone acetate (DepoProvera)
or oral norethindrone (Micronor) would
be appropriate substitutions able to
provide contraception while mitigat-
ing the risk of recurrence.
Vocal cord dysfunction
Vocal cord dysfunction (VCD) refers
to the involuntary paradoxical adduc-
tion of the vocal cords on inspiration.
Other terms for this include paradoxi-
cal vocal cord motion, vocal cord dys-
tonia, laryngeal dyskinesis, vocal cord
adduction, and Münchausen’s stri-
dor.19,20 During an episode of VCD,
inappropriate vocal cord adduction
can lead to inspiratory airflow ob-
struction. This obstruction can cause a
sensation of throat or chest tightness,
air hunger, and stridor. Patients may
also complain of coughing or hoarse-
ness. Vocal cord dysfunction primari-
ly occurs in younger patients (ages 9
to 43 years).21 There is also a gender
bias, with female patients outnumber-
ing males by approximately two to
one. The actual incidence in the gen-
eral population and the athletic popu-
lation is unknown. VCD has been re-
ported in skiing, swimming, track,
cross-country running, figure skating,
boxing, wrestling, soccer, basketball,
football, racquetball, and tae kwon
do.21An athlete with VCD is often mis-
diagnosed as asthmatic, but subse-
quently fails asthma therapy before
further assessment provides the true
diagnosis. As would be expected,
asthma therapy does not help this con-
dition; in fact some asthma treatments
such as corticosteroids, intubation,
and hospitalization may actually harm
the patient.
Typically, VCD features an abrupt
onset and resolution of symptoms.
The pattern of occurrence is generally
variable and not easily reproducible.
VCD sufferers rarely experience arte-
rial desaturation.19-21 Exercise-induced
asthma (EIA) differs from VCD in that
there is no gender bias; symptoms
generally start after 6 to 12 minutes of
exercise and are most severe 5 to 10
minutes after exercise. In addition,
about 50% of subjects are refractory
to repeated exercise challenge for a
period of 2 hours after an episode of
EIA.22 Typically athletes with EIA
respond well to inhaled beta-agonists.
Unfortunately, VCD and EIA can
coexist in athletes.
VCD can be suspected during pul-
monary function testing if there is a
restriction of the inspiratory flow while
symptomatic during exercise testing.
This restriction may present as audi-
tory inspiratory stridor at the time of
testing or as a specific pattern on the
flow-volume loops, with the inspira-
tory curve appearing blunted or flat-
tened. This finding can occur in the
presence or absence of expiratory
flow obstruction. Pulse oximetry is
generally normal. Direct fibre-optic
laryngoscopy is the definitive investi-
gation of choice. It is important that
this be performed while the patient is
symptomatic. To induce symptoms,
patients should carry out a graded
exercise test. Once their symptoms are
present, the challenge is stopped and
laryngoscopy is performed.
Treatment for vocal cord dysfunc-
tion can be difficult. Acute treatment
can involve having the patient pant or
cough. This action seems to resyn-
chronize the respiratory cycle by acti-
vating the vocal cord abductors and
widening the glottic aperture.21 Ad-
ministration of heliox (a helium-oxy-
gen mixture) can also help by reduc-
ing airway turbulence, and therefore
improving airflow through the lar-
ynx.20
Long-term treatment of vocal cord
dysfunction focuses on education and
speech therapy. The goal is to retrain
the patient to breathe appropriately
when under stress. Postural correc-
tion can help to reduce the rounded-
shoulder-neck-forward position, which
can aggravate symptoms. There has
Exertional dyspnea in athletes
Vocal cord dysfunction primarily
occurs in younger patients
(ages 9 to 43 years). There is
also a gender bias, with female
patients outnumbering males by
approximately two to one.

BC MEDICAL JOURNAL VOL. 45 NO. 10, DECEMBER 2003
514
been some suggestion that jaw thrust-
ing during exercise may also reduce
symptoms. VCD can often have a psy-
chological component (such as anxi-
ety secondary to performance expec-
tations), and therefore formal evaluation
may be indicated. Strategies aimed at
reducing the patient’s level of stress
are particularly important. An attempt
should also be made to treat any other
conditions that may irritate the larynx,
such as gastroesophageal reflux dis-
ease and allergic rhinitis.21,23
Conclusion
Pulmonary embolism and vocal cord
dysfunction represent two relatively
uncommon entities that cause exer-
tional dyspnea in athletes and may be
confused with exercise-induced asth-
ma. As the treatment for all three con-
ditions is vastly different, inclusion of
both vocal cord dysfunction and pul-
monary embolism in the differential
diagnosis of exertional dyspnea will
permit earlier diagnosis and more
appropriate management of these con-
ditions.
Competing interests
None declared.
References
1. Weiler JM, Layton T, Hunt M. Asthma in
United States Olympic athletes who par-
ticipated in the 1996 Summer Games. J
Allergy Clin Immunol 1998; 102:722-726.
2. Rupp NT. Diagnosis and management of
exercise-induced asthma. Phys Sports-
med 1996;24:77.
3. Rundell KW, Judelson DA, Williams SD.
Diagnosis of exercise-induced asthma.
In: Rundell KW, Wilber RL, Lemanske RF,
eds. Exercise-Induced Asthma: Patho-
physiology and Treatment. Champaign,
IL: Human Kinetics, 2002:181-209.
4. Mannix ET, Manfredi F, Farber MO. A
comparison of two challenge tests for
identifying exercise-induced broncho-
spasm in figure skaters. Chest 1999;
115:649-653.
5. Wilber RL. Incidence of asthma and exer-
cise-induced asthma. In: Rundell KW,
Wilber RL, Lemanske RF, eds. Exercise-
Induced Asthma: Pathophysiology and
Treatment.Champaign, IL: Human Kinet-
ics, 2002:39-68.
6. Sorkness CA, Kelley R, Lemanske RF.
Asthma treatment and guidelines. In:
Rundell KW, Wilber RL, Lemanske RF,
eds. Exercise-Induced Asthma: Patho-
physiology and Treatment. Champaign,
IL: Human Kinetics, 2002:211-235.
7. McKenzie DC, Stewart IB. Asthma med-
ications as ergogenic aids. In: Rundell
KW, Wilber RL, Lemanske RF, eds. Exer-
cise-Induced Asthma: Pathophysiology
and Treatment. Champaign, IL: Human
Kinetics, 2002:237-256.
8. Brill-Edwards P, Sutton J. Breathlessness
on exertion in a competitive cyclist. Clin
J Sport Med 1991;1:48-52.
9. Croyle PH, Place RA, Hilgenberg AD. Mas-
sive pulmonary embolism in a high school
wrestler. JAMA 1979;241:827-828.
10.Harmon K, Rousch MB. Pulmonary
embolism: Sifting the risk factors. Phys
Sportsmed 1998;26:53-56.
11. Johnson PR, Krafick J, Greene JW. Mas-
sive pulmonary embolism in a varsity ath-
lete. Phys Sportsmed 1984;12:61-63.
12. Tiu S, Srinivasan I, Banner HJ, et al. Break-
dancer’s pulmonary embolism. Clin Nucl
Med 1986;11:402-403.
13.Gaede JT, Montine TJ. Massive pul-
monary embolus and anabolic steroid
abuse. JAMA 1992;267:2328-2329.
14.Greydanus DE, Patel DR. Sports doping
in the adolescent athlete the hope, hype,
and hyperbole. Pediatr Clin North Am
2002;49:829-855.
15. Marx JJ, Vergouwen PC. Packed-cell vol-
ume in elite athletes. Lancet 1998;
352(9126):451.
16.Gomez JE. Upper extremity injuries in
youth sports. Pediatr Clin North Am
2002;49:593-626, vi-vii.
17.Vandenbroucke JP, Rosing J, Bloe-
menkamp KWM, et al. Oral contracep-
tives and the risk of venous thrombosis.
N Engl J Med 2001;344:1527-1535.
18.Weiss G. Risk of venous thromboem-
bolism with third-generation oral contra-
ceptives: A review. Am J Obstet Gynecol
1999;180:S295-S301.
19.Nahmias J, Tansey M, Karetsky MS.
Asthmatic extrathoracic upper airway
obstruction: Laryngeal dyskinesis. N J
Med 1994;91:616-620.
20.Weir M. Vocal cord dysfunction mimics
asthma and may respond to heliox. Clin
Pediatr (Phila) 2002;41:37-41.
21.Brugman SM, Simons SM. Vocal cord
dysfunction—Don’t mistake it for asth-
ma. Phys Sportsmed 1998;26:63-74.
22.Anderson SD, Holzer K. Exercise-
induced asthma: Is it the right diagnosis
in elite athletes? J Allergy Clin Immunol
2000;106:419-428.
23.Powell DM, Karanfilov BI, Beechler KB,
et al. Paradoxical vocal cord dysfunction
in juveniles. Arch Otolaryngol Head Neck
Surg 2000;126:29-34.
Exertional dyspnea in athletes